Shared governance in the plant holobiont and implications for one health

Abstract The holobiont Holobiont theory is more than 80 years old, while the importance of microbial communities for plant holobionts was already identified by Lorenz Hiltner more than a century ago. Both concepts are strongly supported by results from the new field of microbiome research. Here, we present ecological and genetic features of the plant holobiont that underpin principles of a shared governance between hosts and microbes and summarize the relevance of plant holobionts in the context of global change. Moreover, we uncover knowledge gaps that arise when integrating plant holobionts in the broader perspective of the holobiome as well as one and planetary health concepts. Action is needed to consider interacting holobionts at the holobiome scale, for prediction and control of microbiome function to improve human and environmental health outcomes.


Introduction
In 1943, the holobiont theory was already empirically formulated by the German theoretical biologist Adolf Meyer-Abich.In 1991, the famous symbiosis r esearc her Lynn Margulis defined the holobiont a gain, and ob viousl y independentl y of this first description, with the holobiont r epr esenting an association of partners (bionts) throughout a significant portion of the life history (Margulis 1991 ).After the merging of holobiont theory into the hologenome theory of evolution by Zilber-Rosenberg and Rosenberg ( 2008 ), the term has been used more widely and successively applied to different or ganisms, including plants (Vandenk oornhuyse et al. 2015 ).In the last two decades, microbiome research confirmed not only the holobiont theory, it substantially contributed to better insights into host-microbiota relationships and metabolite interplay (Gilbert et al. 2016, Cordovez et al. 2019, Berg et al. 2020 ).The micr obiota, whic h can form div erse micr obiomes in one host, consist of billions of microbial cells from all domains of life (Bacteria, Ar chaea, and Eukary otes: Fungi, and Pr otists) (Ber g et al. 2020 ).Each plant constitutes an individual holobiont comprised of multiple microbiomes that establish in a plant's above-and below-ground tissues .T he differ ent physio-c hemical conditions in those tissues shape the microbiota and form the phyllosphere and rhizosphere (Philippot et al. 2013, Cordovez et al. 2019 ).More than a century a go, Lor enz Hiltner discov er ed the importance of rhizosphere-associated microorganisms for plant growth and health and described all principles of the holobiont concept for plants, ho w e v er, without mentioning the term (Hartmann et al. 2008 ).The rhizosphere describes the soil-plant interface and is crucial for plant micr obiome assembl y and functioning of the plant holobiont (Berg and Smalla 2009 ).The rhizosphere serves as a nexus of communication and metabolic exchange between the plant and the surrounding soil en vironment.Here , we highlight ho w ev olution of the plant holobiont hav e r esulted in a shar ed governance of host and microbiota.Moreover, we address conclusions and knowledge gaps that arise from the broader perspective of one and planetary health.

Evolution and ecology of plant holobionts
Plant evolution is driven in a large part by ancient microbial friends and recent foes (Delaux and Schornack 2021 ).The theory that specific arbuscular mycorrhizal fungi symbionts were drivers of plant terrestrialization in early Palaeozoic land ecosystems, 500-450 million years ago, is well-established but less is known about plant-bacteria interactions during evolution (Brundr ett 2002 ).Nonv ascular plants suc h as liv erw orts, hornw orts, and mosses (bryophytes), the sister lineage to vascular plants, belonged to the first land colonizers (McDaniel 2021 ).Recently it was discov er ed that they harbour a more diverse but less specific micr obiome compar ed to v ascular plants (Wicaksono et al. 2021 ).While vascular plants recruit environmental bacteria thr ough r oot exudates r esulting in plant genotype-specific colonization, bryophytes lack functional roots and maintain their bacterial comm unities thr oughout their lifecycle.Mosses are known for close interaction with mycorrhizal fungi, yet their interaction with prokaryotic microorganisms seems to be highly important as w ell, as sho wn for Funaria (Hornschuh et al. 2006 ), Sphagnum (Br a gina et al. 2012, 2014, Kostka et al. 2016 ), and Riccia (Wicaksono et al. 2023c ).
The ecology of the plant holobiont is an important subject which is still not well-studied.Vertical transmission of the plant microbiota was only recently reported, for mosses via sporophytes (Br a gina et al. 2012 ) and for spermatophytes via seeds (Adam et al. 2018, Johnston-Monje et al. 2016 ).Ho w e v er, both v ertical and horizontal transmission ensure survival of offspring.Particularly the microbiome of seeds has gained scientific attention over the past years due to its benefits for the host plant (Berg and Raaijmakers 2018 ).A r ecent lar ge-scale meta-study on the seed microbiomes of 50 plant species r e v ealed a div erse and flexible seed micr obiome including se v er al high abundant cor e micr obiota (Simonin et al. 2022 ).In general, the vertically transmitted microbiota consist mainly of plant beneficials and symbionts, and the horizontall y acquir ed micr obiota ar e r esponsible for the ada ptation to the local envir onment (Ber gna et al. 2018 ).Plant species can differ in the proportions of vertically and horizontally acquired microbes, yet their contribution to the plant microbiome is in a similar range (Abdelfattah et al. 2023 ), which has been also described for the human microbiome (Hourigan and Dominguez-Bello 2023 ).Ho w ever, the composition of the plant microbiota varies during a plant's life cycle and its assembly is always function-driven (Wicaksono et al. 2021 ).In addition, the microbiota composition follows specific routes; e.g.flo w ers and fruits are being mainly colonized from the endosphere (inside plant tissues) but the development of new organs always allows entrance of pathogens as well (Hardoim et al. 2015, Olimi et al. 2022 ).
What are the functions of the microbiota within the plant holobiont?Plant-associated micr oor ganisms influence the plant already during germination.Certain plant phyla, such as mosses and orc hids, ar e not able to germinate without seed-or soilderiv ed micr obes (Hornsc huh et al. 2006 ).Besides that, micr oorganisms offer a huge array of beneficial functions for plants.For example, the microbiota are involved in the host plant's growth, pr oductivity, ada ptation, physiology, str ess r esilience, and imm unity.Mor eov er, the intense inter action with micr oor ganisms has contributed to diversification within the plant kingdom (Van Der Heijden et al. 2008 ) wher e mor e closel y r elated plant species ar e associated with similar microbial communities; a phenomenon described as phylosymbiosis (Lim and Bordenstein 2020 ).The symbiotic functional interplay can be explained by plant-microbe coevolution forming diverse holobionts.
Coevolution of holobionts suggests a shared governance between the plant and the micr obiome, whic h is supported by the following observations.First, plant germination and plant growth can depend on hormonal interplay with microorganisms.Plantassociated micr oor ganisms pr oduce a v ariety of phytohormones (e .g. auxins , cytokinins , and gibberellins), known for their involvement in germination, root growth, and their ability to modify plant root architecture and growth to increase nutrient uptake (Hornschuh et al. 2006, Vacheron et al. 2013 ).Moreover, they can manipulate stress phytohormone levels, such as plant ethylene le v els by 1-aminocyclopropane-1-carboxylate deaminase .T he establishment of plant-micr obiota r elationships r equir es the exchange of chemical signals and nutrients between the partners.
Ho w e v er, the c hemical signals involv ed ar e lar gel y unknown; plant or micr oor ganism-deriv ed pol yamines ar e one of the important compounds that act as physiological effectors and signal molecules in plant-microbe interactions (Dunn and Becerra-Riv er a 2023 ).Second, plant micr obiome assembl y and r eshuffling is triggered by both, plant and microbes.Recent evidence from genome-wide association studies in plant holobionts r e v ealed host loci with genes involved in plant development, immunity, nutrient uptake, and root exudates that regulate microbiome comm unity structur e (Zhang et al. 2023 ).Third, plant pr otection tow ar ds biotic and abiotic stresses is only achieved by shared governance .Plants ha v e e volv ed a signaling-mediated str ess r esponse to recruit a stress-relieving or protective microbiome, denoted as the 'cry for help of plant roots' (Liu et al. 2021, Mendes et al. 2011 ).Mor eov er, biocontr ol a ppr oac hes hav e r epeatedl y pr ov en that an a pplied biocontr ol a gent inter acts with both, the host plant (induced immunity) and the microbiome (shifts and depletion of pathogens) (Berg et al. 2021, Pieterse et al. 2014 ).A fourth example is fruit or flo w er quality modulation, including flavour, smell, and nutrient contents, which can be a joint venture between plants and their associated microbes that ensures pollination and dispersal.Characteristic flavour compounds of strawberry fruits (Verginer et al. 2010b ) and gr a pe berries (Bokulic h et al. 2014, Verginer et al. 2010a ) were identified to be produced by microbes.

The plant holobiont in the Anthropocene and implications for one health
Climate change has been identified as a core planetary boundary in the Anthr opocene, whic h has the potential to irr e v ersibl y change global systems in the event of insufficient intervention (Lewis andMaslin 2015 , Steffen et al. 2015 ).It is no exaggeration to say that holobionts, plants along with associated micr oor ganisms, lar gel y r egulate Earth's climate and ecosystem response to environmental change.For example, peat mosses of the genus Sphagnum store more carbon that any other plant on Earth; the fate of this carbon is uncertain given climate change (v an Br eemen 1995 ).Plants ar e subject of man y global c hange studies, and v egetation c hanges ar e ob vious all ov er the world (Humphreys et al. 2019, Yang et al. 2021 ).In contrast, the impact of anthropogenic factors, the main drivers of current global ecosystem changes, on the microbiome has received less attention.A recent meta-data and literature study suggested a decline in micr obial div ersity, e v enness, and specificity while the whole microbiome shifts into a dysbiotic stage , i.e .characterized by r-strategists and hypermutator prevalence (Berg and Cernava 2022 ).This corresponds to an increased abundance but reduced div ersity of antimicr obial r esistance genes, as shown for differ ent built environments with increasing grade of anthropogenic influences (Mahnert et al. 2019 ).Altogether, the abundance and activity of symbiotic micr oor ganisms a ppears to be declining, while the number of pathogen outbreaks is increasing.Moreover, Delgado-Baquerizo et al. ( 2020 ) provided predictions for the introduction of ne w pathogens, mainl y fungi, into pr oduction ar eas that hav e r emained spar ed so far.Ov er all, inv estigations that incor por ate a holistic view of the functional implications of shared governance are missing (Cavicchioli et al. 2019 ).
While holistic and mechanistic studies on the plant holobiont are rare, initial studies investigating the impact of climate driv ers (warming, ele v ated atmospheric CO 2 ) on the plant holobiont show alarming results .T he Spruce and Peatland Responses under Changing Environments (SPRUCE; https://mnspruce.ornl.gov/) experiment is a whole-ecosystem warming ( + 0 • C to + 9 • C) and ele v ated atmospheric CO 2 (eCO 2 ; + 500 ppm) experiment conducted in a r egr ession design to test the impacts of climate drivers on ecosystem response in a Sphagnum -dominated ombrotrophic peatland.Results from this experiment indicate that warming causes dysbiosis in the Sphagnum phytobiome (i.e. the plant together with its constituent microbiome within the environment), as evidenced by a decline in microbial diversity, a pronounced shift in community composition including diazotrophs, and a decline in nitrogen fixation rates (Carrell et al. 2019 ).Northern peatlands are often nutrient-poor and thus nitrogen fixation or diazotrophy often comprises a large portion of plant demand for nitrogen in these systems (Salmon et al. 2021, Warren et al. 2017 ).Diazotrophs of the Sphagnum microbiome couple nitrogen fixation to methanotr ophy, ther eby consuming the potent greenhouse gas methane before it is released to the atmosphere (Kolton et al. 2022, Larmola et al. 2014, Vile et al. 2014 ).A recent study b y P etro et al. ( 2023) at the SPRUCE site sho ws that this coupling of the nitrogen and carbon cycles in the Sphagnum microbiome is short circuited by climate drivers.Under ambient CO 2 , warming incr eases plant-av ailable NH 4 -N in surface peat, excess N accumulates in Sphagnum tissue, and N 2 fixation activity decr eases.Ele v ated CO 2 offsets the effects of warming, which disrupts the accumulation of N in the peat and Sphagnum tissues.Methane concentrations in porewater increases with warming, irr espectiv e of CO 2 tr eatment.Under + 9 • C, this r esults in a 10fold higher methanotrophic activity in the Sphagnum microbiome.W arming' s div er gent impacts on diazotr ophy and methanotr ophy caused these processes to become decoupled at warmer temperatur es, as e videnced by declining r ates of methane-induced N 2 fixation and significant losses of k e ystone microbial taxa.In addition to changes in the Sphagnum microbiome, ∼94% mortality of Sphagnum was observed between the + 0 • C and + 9 • C treatments, possibly due to the collective impacts of warming on N-availability and competition with emer ging v ascular plant species.Altogether, rising temper atur es and atmospheric CO 2 concentr ations ar e expected to result in a vegetation shift r eferr ed to as 'shrubification' (Malhotr a et al. 2020 ), wher eby shrubs and tr ees r eplace Sphagnum mosses-the engineers and masters of carbon stor a ge-with significant implications for carbon and nitrogen cycling in boreal peatlands.In parallel, peat decomposition is boosting climate change: as peatland vegetation trends to w ar d increasing vascular plant cover with warming, the massive carbon stores in peatlands ar e vulner able to degr adation (Hopple et al. 2020 ) and we can expect a concomitant shift to w ar ds incr easingl y methanogenic conditions and amplified climate-peatland feedbacks (Wilson et al. 2021 ).In addition, carbon substrate utilization is limited by the availability of terminal electron acceptors and porewater dissolv ed or ganic matter, and these controls of microbial peat soil organic matter degradation are dependent on the temperature (Song et al. 2023 ).Another warming experiment on oak seedlings, carried out under controlled conditions, provided clear evidence that higher temperatures reduce the diversity of oakinhabiting fungi with influence on the holobiont's health (Faticov et al. 2021 ).
Recently, the plant microbiome was included in the one health concept (Flandroy et al. 2018 ).During the last years, human infections caused by bacterial and fungal pathogens originating from plants has r eceiv ed attention (Ber g et al. 2005, Ber endonk et al. 2015, Kim et al. 2020 ).Gener all y, these micr obes can be divided into two groups: human pathogens that cause severe food-borne diseases through association with the plant as an alternative host, and opportunistic pathogens that cause most of the healthcareassociated infections (HCAIs) world-wide (Kim et al. 2020 ).While the first group is deeply studied and well integrated into food safety concepts , HC AIs of plant or en vir onmental origin ar e less understood and difficult to avoid (Kim et al. 2020 , Yoon andLee 2018 ).In general, HCAIs have a severe impact on human health: more than 4 million and 1.7 million patients are affected by HCAIs e v ery year in Europe and in the USA, r espectiv el y.Although less so in middle-and low-income countries, in high-income countries, ∼30% of ICU patients are affected by at least one episode of HCAI (WHO 2011 ).HCAIs of plant origin typically occur in immunocompr omised, postsur gical, or post-tr aumatic patients, categorizing them as opportunistic pathogens without specificity (Berg et al. 2005, Kim et al. 2020 ) but they are often characterized by their high potential for antimicrobial resistance (Berendonk et al. 2015 ) .Antimicr obial r esistance is necessary for microbes to colonize plants, especially in the rhizospher e, wher e antimicr obial compounds are often secreted; under antibiotic pressure in health-car e settings, those micr obes ar e selectiv el y enric hed (Ber g et al. 2005 ).
The WHO priority list for pathogens with high antimicrobial r esistance, whic h ar e difficult to contr ol and need ur gent attention (WHO 2017 ), comprise the se v er al bacterial species, whic h are w ell-kno wn for their fr equent occurr ence and positiv e interaction with plants.In the following list, plant-associated micr obes ar e highlighted in bold: Priority 1: CRITICAL: Acinetobacter baumannii , Pseudomonas aeruginosa , and Enterobacteriaceae , Priority 2: HIGH: Enterococcus faecium , Staphylococcus aureus , Helicobacter p ylori , Camp ylobacter spp ., Salmonellae , and Neisseria gonorrhoeae , Priority 3: MEDIUM: Streptococcus pneumonia , Haemophilus influenza , and Shigella spp .This is confirmed by a systematic analysis for the Global Burden of Disease Study 2019, which identified 33 global bacterial pathogens and five pathogens that were eac h involv ed in mor e than 500 000 deaths in 2019: S. aur eus , Esc heric hia coli , S. pneumoniae , K. pneumoniae , and P. aeruginosa .Pseudomonas aeruginosa is a frequent inhabitant of the rhizosphere, e.g. the rhizosphere of potato, strawberry, oilseed rape, rice, and wheat (Berg et al. 2005 ), and strains of this species are often selected as excellent biocontr ol a gents a gainst plant pathogens (Wang et al. 2020, Yasmin et al. 2017 ).Earlier studies reported potential human pathogens in the rhizosphere of wheat grown on soils with high salt concentration (Egamberdieva et al. 2007 ).Salt-tolerant Staphylococcus species, commonly known as potential human or animal pathogens , ha ve also been observed in the rhizosphere of saltwort (Shurigin et al. 2020 ).High salt concentrations and soil temper atur es in dry areas will foster favourable circumstances for bacteria that have their origins in warm-blooded animals .T he family Enterobacteriaceae is a specific group which colonize abov e-gr ound plant parts and inner compartments of (healthy) seeds (Lindow and Brandl 2003, Rossmann et al. 2012, Simonin et al. 2022 ).It was observed that the intraspecific diversity of Enterobacteriaceae in pumpkin seeds is a health indicator for seed and plants in the field (Adam et al. 2018 ).These examples show that emerging human pathogens with antimicr obial r esistance pr ofiles can be associated to plants.Se v er al of them are known for their plant-beneficial interaction, and are thus of interest for biotechnological applications .T he functions and ambiv alent inter actions with differ ent hosts m ust be studied intensiv el y and a pplication or commercialization of potential (opportunistic) human pathogens should be car efull y assessed or restricted.
It is imper ativ e to thor oughl y anal yze another significant aspect, namel y the ov erla p of bacterial taxa found in plants that possess the potential to cause infections in humans .T his examination will determine if these taxa possess identical c har acteristics across both domains .T he plant microbiome can act as reservoir for opportunistic, often multiresistant pathogens .T his can be explained by the ecology of the plant holobiont and its sessile lifestyle producing secondary metabolites with antimicrobial activity.For successful plant colonization of an endophyte, all steps-r ecognition, adher ence , in vasion, and establishmentar e r equir ed; the same ar e r equir ed by pathogens (Ber g et al. 2005 ).Se v er al bacterial gener a, including Bur kholderia , Enterobacter , Pseudomonas , Ralstonia , Staphylococcus , and Stenotrophomonas , contain plant-associated strains that can have different effects on both plants and humans.(Berg et al. 2005 ).While opportunistic bacteria from plants do have some properties in common, each of these opportunistic pathogens has its own features, summarized, e.g. for P. aeruginosa (Laborda et al. 2022 ) and Stenotrophomonas maltophilia (Lira et al. 2017 ).Another example is Shigella; r ecentl y, human-pathogenic bacteria Shigella boydii and S. flexneri were found to colonize leaves and roots of Arabidopsis .Further studies r e v ealed that the Shigella type III secretion system not onl y r egulates the pathogenesis of shigellosis in humans but also plays a central role in bacterial proliferation in the plant, for which the immunosuppressi ve acti vity of two type III effectors, OspF and OspG, was r equir ed (Jo et al. 2019 ).Although bacteria are considered as major burden, there are also examples for fungal pathogens .T he fungus Chondrostereum purpureum , known to cause Silver leaf disease of plants, particularly of the rose family, was previously not considered a threat to humans.Ho w e v er, a r ecent r eport has documented the first case of a par atr ac heal abscess in humans caused by C. purpureum (Dutta and Ray 2023 ).Altogether, viral, bacterial, and fungal pathogens of plants and animals can adapt to both abiotic and biotic factors of the Anthropocene, including climate change (Cavicchioli et al. 2019, Giraud et al. 2017 ).Mor eov er, a gricultur al ecosystems share global features, and the dispersal of pathogens through human tr av el and plant material transport enhances the potential of pathogens to broaden both, the environmental and the host r ange, e v en cr oss-kingdom, and incr ease their c hances to enter hospital en vironments .T he molecular mechanisms behind cross-kingdom infections remain unclear, but should be studied in detail to determine mechanisms for disease pr e v ention (Kim et al. 2020 ).
While the biodiversity hypothesis/missing microbe theory is well-established in the context of human health (Blaser 2017, Finlay et al. 2021, Hanski et al. 2012 ), plant health has r eceiv ed less attention in this regar d.Ho w ever, the transformation of the plant microbiome in the Anthropocene , i.e .declined microbial div ersity, e v enness, and specificity, and increased abundance of r-str ategists, hyperm utators, and antimicr obial r esistance, indicates that plant health is already being remarkably affected.Micr obiome-based contr ol concepts ar e an inter esting alternativ e to curr ent pesticides, fertilizers and disinfectants (Vandini et al. 2014 ).Plant and environmental health are directly linked to human health which becomes clear from the unintended consequences of intense a gricultur e in the former Aral Sea region (Wicaksono et al. 2023b ) and destructive mining practices in the Salares of the hyperarid Atacama Desert in Northern Chile (Bonelli and Dorador 2021 ).Another link between human health and the depleted plant micr obiome, especiall y the "edible microbiome", was already suggested in 2015, which needs further e v aluation (Berg et al. 2015, Wicaksono et al. 2023a ).

Conclusions
In the last two decades of micr obiome r esearc h, the holobiont theory and the hologenome theory of evolution were confirmed, ther eby r e v ealing ne w insights into coe volution and shar ed governance of eucaryotic hosts and their associated microbiomes.Here, we describe the implications for plant holobionts and their response to ongoing global environmental changes.Importantly, they are integrated into ecosystems and interact with other holobionts, designated as holobiomes or meta-communities (Bragina et al. 2015 ).Holobiome is a term used for different purposes but, according to the origin of the word it combines micro-and macrobiomes into the holobiome [Holobiome .T he w or ds "holo" and "biome" are of Ancient Greek origin."Holo" Hólos < όλoς> means whole, while the term "biome" is composed of the Greek w or d bíos ( βιoς , life) and modified by the ending "ome" (Anglicization of Greek)].Ho w ever, anthropogenic activities have changed the signature of the environmental and host-associated microbiomes, resulting in severe health problems in the holobiome.Action is needed to protect plant holobionts as the centerpieces of the holobiome, with major implications for human and environmental health on a r a pidl y c hanging Earth.
Holobiont r esearc h catal yzes ne w a ppr oac hes and a r ethinking of current practices .Here , we pro vide the following examples: r The role of mycorrhizal fungi symbionts as evolutionary drivers of plants' colonization of land ecosystems and diversification is well-established but less is known about the other members of the plant microbiome during evolutionunderstanding can boost microbiome-supported agriculture.
r Breeding shifted the plant microbiome to a similar extent than the crop phenotype.Microbiome-based breeding can maintain the symbiotic and beneficial part of the plant microbiome .Here , understanding the physiology and harnessing the functional potential of the seed microbiome will help to de v elop sustainable a ppr oac hes and pr ovide crucial insights into plant microbiome coevolution.
r Vertical transmission and horizontal acquisition of the plant micr obiome ar e crucial for holobiont's resilience.Micr obiome-based plant pr otection str ategies can be de v eloped to avoid outbreaks of pathogens and pests.
r A healthy plant is c har acterized by a microbiome , i.e .diverse in structure and function; functional diversity matters.Instead of reducing microbial diversity, e.g. by seed treatments and in a gricultur e in gener al, ne w a ppr oac hes that enric h micr obial div ersity should be implemented.Micr obiome management by abiotic (organic materials and humic acids) and biotic (microbial seed coatings , transplants , and biocontrol) treatments can help to develop resilient plants.
r The plant microbiome plays a crucial role in the one health concept, as reservoir for food pathogens as well as opportunistic, often m ultir esistant pathogens that cause HC AIs .Especially for the latter, new microbiome-based control concepts are essential.Certainly, new antibiotics and disinfectants are very important in hospital environments and disease treatments; in the long-term and on environmental scale, we must rethink current practices.
r Plants with its diverse coevolved plant microbiome is cru- cial for planetary health.Plant holobionts drive global biogeochemical cycles and mediate planetary resilience in the face of massive and ongoing environmental changes .T he adaptiv e mana gement and r estor ation of ecosystems in r esponse to global change should include holobiont-based strategies.
r Interdisciplinary and holistic a ppr oac hes that consider shar ed gov ernance as a principle for all holobionts ar e inevitable to save the planet.
Our joint discussion identified the following knowledge gaps: r The structure and function of the holobiont is well-studied but communication and interaction between the host and the micr oor ganisms as well as the entir e micr obiome is less understood.Inter-and intraspecific communications by volatile organic compounds, small molecules, membr ane v esicles (exosome), or sound vibration represent particularly intriguing areas that warrant further research.
r Viruses ar e driv ers of the micr obiome e volution.At the same time, they are an often neglected component, which needs more attention.
r Holistic a ppr oac hes should also include information fr om southern hemispher e ecosystems, whic h ar e less r epr esented in the liter atur e.
r The one health concept is based on interconnected holo- bionts.While transmission of pathogens between different hosts and environments is well-investigated, less is known for beneficial micr oor ganisms.
r The exposome can be defined as the measure of all (physi- cal, biological, and c hemical) exposur es of an individual in a lifetime and how those exposures relate to health.The plant and environmental microbiome is not yet considered in the concept but must be implemented as well.Especially food as micr obial tr ansmission r oute to the human gut ("the edible microbiome") needs further studies.
r Nonfood plant holobionts that drive the global carbon cycle and provide critical ecosystem services, are severely understudied.
r Genotype-phenotype relationships are not understood at the holobiome scale.
r We need to advance understanding of how microbiomes control the physiological ecology of plant holobionts at the ecosystem scale (cotranscriptomics).